Perceptions, attitudes and practices regarding canine zoonotic helminthiases among dog owners in Nyagatare district, Rwanda

Abstract Background Despite their importance to society, dogs are susceptible to various helminths. This study aimed to understand perceptions, attitudes and practices (PAP) regarding canine zoonotic helminthiases (CZH) among dog owners in Rwanda. Methods A cross‐sectional study was carried out in Nyagatare district of Rwanda, where 203 dog owners were randomly selected and interviewed. To analyse this study's data, we used frequency distributions, chi‐square test of association and binary logistic regression model. Results Overall, 75.9% and 30% of the respondents were aware of canine and human helminthiases, respectively. Around 74.4% knew that dogs source helminthiases from eating raw infected meat. Also, 74.4% knew vomiting, diarrhoea and swelling of the belly as clinical signs of the helminthiases. Around 58.6% washed hands with soap and water after handling a dog. Only 17.2% and 15.5% dewormed the dogs and treated them against ectoparasites using conventional anthelmintics and acaricides manufactured for dogs, respectively. Of all respondents, 33% held genuine perceptions, while 78.3% and 25.1% adopted positive attitudes and appropriate practices about CZH, respectively. The respondents’ educational level and length of dog ownership correlated with their perceptions and practices about CZH, respectively, while sources of information on CZH influenced their PAP of such infections. The adjusted odds ratio (OR) of having genuine perceptions and positive attitudes were more than 82% lower among those who sourced the information from neighbours & colleagues compared to those who gathered it through reading. Again, the length of dog ownership (OR = 0.37, 95% CI: 0.15–0.90) correlated with the respondent's practices about CZH. Conclusions Only 33% and 25.1% of the respondents held genuine perceptions and adopted positive attitudes regarding CZH, respectively. The findings indicate increased zoonotic helminths in dogs, possible spillover in humans and anthelmintic resistance. Therefore, awareness campaigns are needed to upgrade dog owners’ knowledge of the zoonotic helminthiases in dogs in Nyagatare district.


INTRODUCTION
Dogs are valued animals in human society and the role they play has gradually changed to include hunting and guarding, offering services and companionship (Beck et al., 2012;Wells, 2007). Despite their roles, they also harbour a wide range of helminths including nematodes, trematodes and cestodes (El-Gayar, 2007;Sharma et al., 2017) and some are zoonotic such as Ancylostoma spp, Toxocara canis, Echinococcus spp and Dipylidium caninum (Jiang et al., 2017;Moskvina & Ermolenko, 2016). Some helminths are also responsible for neglected tropical infections, for example, Ancylostoma spp and Echinococcus spp (Engels & Zhou, 2020).
Dogs get ancylostomiasis via oral ingestion or skin penetration of infective larvae. Oral transmission involves ingesting infected milk, paratenic hosts or suckling infected dams (Ballweber, 2001). In dogs, toxocariasis is transmitted via ingesting faeces or soil loaded with embryonated eggs or suckling infected dams. Pregnant bitches can also transmit the infection to foetuses (Despommier, 2003). Although Felidae and Hyaenidae can be definitive hosts for Echinococcus spp, domestic dogs and other Canidae are the main definitive hosts (Romig et al., 2017). Both herbivores and omnivores are intermediate hosts and dogs get infected when they eat meat from infected intermediate hosts (Romig et al., 2017;Vass & Nappi, 2002). Dogs can also act as aberrant intermediate hosts for E. multilocularis and develop alveolar echinococcosis (Frey et al., 2017;Haller et al., 1998). Dogs develop the latter infection when they consume food, water or faeces contaminated with E. multilocularis eggs or autoinfect themselves when adult worms of E. multilocularis present in their intestines lay eggs (Frey et al., 2017;Scharf et al., 2004). Of ten species of Echinococcus currently known, seven are zoonotic (Thompson, 2020). Dogs develop dipylidiasis after ingesting an intermediate host (fleas) containing an egg capsule of D.
Humans can directly contract zoonotic helminths from animals or their products (e.g. Trichinella spiralis) or can indirectly get infected through invertebrate or vertebrate intermediate hosts and contaminated items such as soil and water (Youn, 2009). Humans infected with some zoonotic helminths for example Strongyloides stercoralis can also autoinfect themselves (Stepek et al., 2006). Humans develop Toxocara canis infection when they ingest items loaded with embryonated eggs while they contract hookworm (Ancylostomatidae) infections through oral or percutaneous routes (Despommier, 2003;Sharma et al., 2017).When they touch an infected dog, humans can accidentally ingest Echinococcus spp eggs and develop the infection. (Roberts et al., 2009). Humans can also develop dipylidiasis once they accidentally ingest infected dog and cat fleas (Despommier et al., 2019). If exposed cysticercoids are present on a dog tongue after grooming, the dog may also transmit dipylidiasis to people through licking them (Sapp & Bradbury, 2020).
In a study conducted in dogs in Rwanda, the prevalence of Ancylostoma spp was 32.3% while that of Toxocara canis and Ancylostoma spp coinfection represented 1.1% (Ntampaka et al., 2021). Another study conducted in school children in Rwanda reported the prevalence of hookworms of 1.9% (Kabatende et al., 2020). Dogs suffering from toxocariasis manifest different signs including poor hair coat, general unthriftiness, slow weight increase, vomiting and diarrhoea (Ballweber, 2001;Sharma et al., 2017). The clinical picture of canine ancylostomiasis includes bloody diarrhoea and chronic anaemia in puppies and adult dogs, respectively (Sharma et al., 2017).
Although dogs suffering from dipylidiasis do not exhibit any clinical disease, some dogs can have diarrhoea and anal pruritis (Ballweber, 2001;Saini et al., 2016). Dogs having intestinal echinococcosis caused by adult worms do not show clinical signs (Haller et al., 1998). The control of canine dipylidiasis involves deworming dogs and combatting fleas, especially in households (Jiang et al., 2017). Canine ancylostomiasis, toxocariasis and echinococcosis can be controlled via prophylactic deworming (Ballweber, 2001). In addition, the prevention of echinococcosis requires preventing dogs from scavenging and predating wherever possible (Romig et al., 2017).
In Rwanda, dog owners purchase anthelmintics formulated for dogs from veterinary pharmacies and ivermectin, Ascaten-P (contains mebendazole, piperazine citrate and praziquantel) and Univerm total (includes praziquantel, pyrantel embonate and fenbendazole) are examples of the drugs that were available at the time of this study.
To the best of our knowledge, no published study has investigated the level of awareness, perceptions and practices about canine zoonotic helminthiases among dog owners in Rwanda and thus, this information is lacking. It is unknown whether dog owners are knowledgeable about the potential health risks associated with dogs, especially canine zoonotic helminthiases. A study conducted in Ghana found that 60% of dog owners were aware of canine helminthiases (Amissah-Reynolds et al., 2016). The same study also reported that 24% knew that dogs could spread zoonotic parasites to humans and that 13% adopted appropriate practices of dog feeding (feeding them in a bowl) while 46% never dewormed their dogs. Previous studies reported a level of awareness of transmission of zoonotic parasites from dogs to humans that varied between 4.6%−10% (Kiflu et al., 2016;Panigrahi et al., 2014).
Therefore, this study aimed to understand the perceptions, attitudes and practices regarding CZH among dog owners in Nyagatare district, Rwanda.

Study area
This study was conducted in Nyagatare district between May and July 2019. Nyagatare is one of 30 administrative districts of Rwanda.
The district is in Eastern province of Rwanda and it borders Uganda in the North, Tanzania in the East, Gatsibo district in the South and Gicumbi district in the West. Nyagatare district is also divided into 14 administrative sectors and each one is subdivided into administrative cells and as a whole, the district covers 106 cells. First, Nyagatare district was purposively selected because it is a district dedicated to farming and has the highest cattle population in Rwanda. Given that many dairy cattle farmers also keep guard dogs, we wanted to assess whether the farmers are aware of the potential health risks associated with dogs, especially canine zoonotic helminthiases. Second, Nyagatare sector was selected as it was home to the largest dog population in the district. Given Nyagatare city is also among the six secondary cities in Rwanda; it is rapidly growing and dog ownership has been on the rise (World Bank Group, 2017).
The current study covered six of the nine administrative cells of Nyagatare sector including Nyagatare, Barija, Nsheke, Ryabega, Rutaraka and Bushoga. The remaining three cells were home to a very small dog population and were not included in this study. The map of Nyagatare sector and the study area is shown (Figure 1). Figure 1 shows Nyagatare administrative sector (red boundaries) and its nine administrative cells. The map was generated using ArcGis10.2 software based on shapefiles available at DIVA-GIS (Hijmans, 2012).

Study design and sample size
We conducted a cross-sectional study involving structured questionnaire-based interviews with dog owners living in Nyagatare sector. In 2019, Nyagatare sector-registers indicated a population of 800 dogs. Although the dog population would be slightly more than the households owning dogs, we assumed that every household owned one dog. Thus, this study considered 800 households to represent a reasonable population size of dog owners for calculating the sample size of participants. By the time of this study, there was no published work on perceptions, attitudes or practices of canine zoonotic helminthiases in Rwanda, thus a theoretical proportion of 50% was used to maximise the sample size (Bartlett et al., 2001). Allowing a maximum estimation error of 5% and a confidence intervals of 95%, the sample size was determined using Cochran formula for sample size for categorical data (Bartlett et al., 2001). Therefore, a representative sample of 203 households was required for this study. Using the listing of dogs, the first dog was randomly chosen and the other 202 dogs were picked out by systematically selecting every third dog on the list.
Considering the population of 800 and sample size of 203, i = 800/203 = 3.9. In a circular sampling, we typically round down that is to 3. With the help of local leaders, the owners of the selected dogs were subsequently visited at their households for interviews.

Data collection
A questionnaire consisting of both closed and open questions was specifically designed for this study and it was pretested before interviewing the respondents. During the pretest, the questionnaire was administered to seven dog owners who were randomly contacted and interviewed for judging it: the raised weaknesses were worked on. The questions focused on PAP regarding CZH among dog owners in Nyagatare administrative sector. Each interview lasted for about 15 minutes and the respondents provided answers in Kinyarwanda and these were translated back in English before cleaning and analysing the data.
During data collection and analysis, each respondent's data records were identified with a unique code.

Data analysis
All the participants' answers to survey questions were classified as either correct (scored with 1) or wrong (scored with 0) (Alrubaiee et al., 2020;Della Polla et al., 2020;ul Haq et al., 2012

Sociodemographic characteristics of respondents
Overall, 203 participants were recruited into this study and they were of different background in terms of age, sex, education, occupation and length of dog ownership. Of all respondents, 100% were dog owners and 93.1% kept dogs for security reason. Nearly 62.1% did farming and 61.6% sourced information about canine helminths from colleagues and neighbours (Table 1).

2.6
Respondents' perceptions about canine zoonotic helminthiases Approximately 75.9% of the respondents perceived that dogs could develop helminthiases and 74.4% were aware that dogs can get infected through eating raw infected meat. Only 8.9% recognised that dogs can contract the infections through ingesting ectoparasites (fleas). The percentage of respondents who perceived that dogs could transmit helminthiases to people and the correct routes through which humans can contract such infections represented 30% each. Vomiting, diarrhoea and swelling of belly were the known clinical signs accounting for 74.4%. The proportion of the respondents who held genuine perceptions on CZH represented 33% (Table 2).
The results in Table 3 indicate that the proportion of dog owners who had genuine perceptions was higher in those who completed secondary school (34.3%) compared to other educational levels.
Further, the proportion of dog owners who held genuine perceptions was higher in respondents who sourced information on CZH through personal reading (42.6%) compared to other sources of information.

Respondent's characteristics Frequency Percentage
Age group

Practices relating to the control of canine zoonotic helminthiases
Of all respondents, 33.5% and 29.6% adopted appropriate practices of feeding and of dog deworming, respectively. Only 5.4% of those who dewormed their dogs (n = 60) adopted appropriate practices about the diagnosis of helminthiasis before deworming. Around 17.2% and 15.8% adopted appropriate practices regarding the treatment against helminths and ectoparasites, respectively. Ascaten-P ® was the most used combination (12.3%), followed by Ivermectin (3.4%) and Univerm total ® (1.5%) was the least used combination (Table 5). The proportion of the respondents who adopted appropriate practices regarding CZH accounted for 25.1% (Table 6). The results in Table 5 show that the proportion of dog owners who adopted appropriate practices about CZH was higher in those who received tertiary education (33.3%) compared to those who completed lower educational levels. Again, it was higher in those who were involved in activities other than farming (52.9%).
It was also higher in dog owners who acquired information on CZH through person reading (37.3%) compared to those who got information from other sources.

2.6.3
Chi-square test of associations of the respondents' perceptions, attitudes and practices about canine zoonotic helminthiases The respondents' educational level and sources of information on canine zoonotic helminthiases correlated with their perceptions, attitudes and practices of such infections in Nyagatare. Besides, their occupation correlated with attitudes and practices and the length of dog ownership also positively influenced the respondents' practices of canine zoonotic helminthiases in Nyagatare (Table 3).

Logistic regression analyses
We modelled the probability of responding correctly to at least 50% of the questions using a multivariable binary logistic model. The results in Table 6 show that the OR of having genuine perceptions about canine zoonotic helminthiases for those who completed tertiary education were more than five times higher than the odds for those who had no formal education. Also, the respondents' sources of information on canine zoonotic helminths correlated with their perceptions, attitudes and practices regarding the infection. Specifically, the adjusted OR of having genuine perceptions and positive attitudes were more than 82% lower among those who sourced the information from neighbours and colleagues compared to those who gathered it through reading. Again, the length of dog ownership (OR = 0.37, 95% CI: 0.15-0.90) correlated with the respondent's practices regarding the zoonotic helminthiases in dogs. Specifically, the odds of adopting appropriate practices of canine zoonotic helminthiases were 63% lower among those who kept dogs for 1-3 years than the odds for those who owned dogs for less than a year.

DISCUSSION
This study aimed to understand the perceptions, attitudes and prac- identified that dogs spread helminthiases to humans and the proportion was higher than 10% and 7.4% reported in India and Nigeria, respectively (Panigrahi et al., 2014;Ugbomoiko et al., 2008). However, it was lower than 55% revealed in Canada (Stull et al., 2012).
The methods of getting information on CZH among the respondents might have negatively impacted the proportion of those who held genuine perceptions. Our respondents mainly sourced the information from friends and colleagues, while the respondents interviewed by Stull et al. in Canada mainly received information from veterinarians.
Maybe, when dog owners sought information from veterinarians, they received accurate information on CZH while they got little information when they received it from colleagues and friends. In Rwanda, veterinary training started a few years ago; the number of veterinarians is still insufficient and the penetration of veterinary services is not commendable (Brown et al., 2020;World Organisation for Animal Health, 2019). Such circumstances would predispose dog owners and farmers towards sourcing animal health information from their peers rather than veterinarians. The 61.6% of our respondents who acquired infor-mation on canine zoonotic helminths from colleagues and friends was higher than 48% found in Ethiopia (Kiflu et al., 2016). Again, 14.3% of those who sourced it from professionals, including veterinarians, was lower than 18.6% (Kiflu et al., 2016). Although veterinary education in Ethiopia started many years ago compared to that of Rwanda (Brown et al., 2020), this indicates that sources of animal health information vary between locations. Sourcing information regarding CZH from colleagues and friends can result in sharing inaccurate information and predisposing dog owners to adopting inappropriate practices against such infections.
We found that 58.6% of the respondents would wash hands with water and soap after handling a dog and this was lower than 78.8% who washed their hands after touching a dog in Ethiopia (Kiflu et al., 2016). Hand washing is a good practice of mitigating zoonotic infections (Stull et al., 2012;Wong & Lee, 2019) and adopting it (e.g. using water and soap) would remove dirt, including dog-spread helminth eggs from human hands. Our findings showed that 33.5% of the respondents fed their dogs in utensils and the figure was higher than 13% reported in Ghana (Amissah-Reynolds et al., 2016). Feeding dogs on the bare ground can predispose them to helminthiases. For instance, canine toxocariasis can be transmitted through ingesting soil loaded with embryonated eggs (Despommier, 2003).
We found that 17.2% of the respondents dewormed their dogs using conventional anthelmintics. This percentage was higher than that reported in Ethiopia, where not a single respondent applied conventional anthelmintics (Kebede, 2019). It was however lower than 50.9% reported in Ghana (Johnson et al., 2015). Around 12.3% of our respondents dewormed their dogs with herbal medicine and the percentage was lower than 39% in a study conducted in Ethiopia (Kebede, 2019).
Rwandan traditional healers use Phytolacca dodecandra vernacularly known as Umuhoko as a taenifuge and Clutia abyssinica vernacularly known as Umutarishonga as ascarifuge (Ramathal & Ngassapa, 2001). In this study, only 5.4% dewormed their dogs after the diagnosis. The application of anthelmintics without performing the diagno-sis could progressively lead to anthelminthic resistance (Pullola et al., 2006). Approximately 15.8% treated their dogs against ectoparasites using acaricide formulations manufactured for dogs. The rest did (or not) spray theirs after treating cattle or small ruminants (sheep/goats) against ectoparasites. The application of acaricide manufactured for cattle in dogs could fail the product (Coles & Dryden, 2014). Our findings are of public health importance and adopting one health approach would help control human helminths. This study has some limitations: its design did not allow to determine the level of knowledge of the dog owners about zoonotic helminths in dogs rather their perceptions. TA B L E 6 Logistic regression analyses of the factors associated with PAP among dog owners in Nyagatare, Rwanda (n = 203)

Perceptions
Attitudes Practices

CONSENT STATEMENT
The owner of this case has consented to the disclosure of this case's information.

DATA AVAILABILITY STATEMENT
The data that support the findings of this study are available from the corresponding author upon reasonable request.